Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1987 Dec;394:481–499. doi: 10.1113/jphysiol.1987.sp016882

Characteristics of transmural potential changes associated with the proton-peptide co-transport in toad small intestine.

M Abe 1, T Hoshi 1, A Tajima 1
PMCID: PMC1191973  PMID: 3443974

Abstract

1. Ionic dependence and kinetic properties of the peptide-evoked potentials across everted toad intestine were investigated with eighteen dipeptides and four tripeptides. All peptides evoked saturable increases in the mucosal negativity regardless of the presence of Na+. 2. The peptide-evoked potentials recorded in the absence of Na+ were sensitive to external pH (pHo); lowering pHo from 7.4 to 6.5 and 5.5 caused stepwise increases in their amplitude. 3. Loading epithelial cells with 9-aminoacridine or acetate caused a significant increase or decrease in amplitude of the Gly-Gly-evoked potential, suggesting intracellular alkalinization or acidification also has a great influence on the peptide-evoked potential. 4. Kinetically, Na+-independent peptide-evoked potentials conformed to simple Michaelis-Menten kinetics, and lowering pHo caused a decrease of the half-saturation concentration (Kt) for Gly-Gly without changing the maximum potential difference increase. Similar affinity-type kinetic effect was also seen for Gly-Gly influx. 5. Simultaneous measurements of Gly-Gly-induced increase in short-circuit current and Gly-Gly influx revealed that the coupling ratio of H+ and Gly-Gly flows was 1.78 +/- 0.12, suggesting the stoichiometry of the H+-peptide co-transport being 2:1. 6. Kinetic analyses of the peptide-evoked potentials indicated that all glycyl-dipeptides tested (Gly-Gly, Gly-Pro, Gly-Sar, Gly-Leu, Gly-Phe) and other dipeptides (Ala-Ala, Ala-Phe, Phe-Ala) shared a common carrier. Gly-Gly-Gly and Ala-Ala-Ala were also found to share the same carrier, while Phe-Phe, Leu-Leu and Phe-Leu appeared to be transported by a different carrier. 7. Kt values for di- and tripeptides, which apparently shared a common carrier, fell in a narrow range (0.5-2.2 mM). There was no clear correlation between 1/Kt value and molecular weight.

Full text

PDF
481

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Addison J. M., Burston D., Matthews D. M. Evidence for active transport of the dipeptide glycylsarcosine by hamster jejunum in vitro. Clin Sci. 1972 Dec;43(6):907–911. doi: 10.1042/cs0430907. [DOI] [PubMed] [Google Scholar]
  2. Addison J. M., Burston D., Matthews D. M., Payne J. W., Wilkinson S. Proceedings: Evidence for active transport of the tripeptide glycylsarcosylsarcosine by hamster jejunum in vitro. Clin Sci Mol Med. 1974 Jun;46(6):30P–30P. [PubMed] [Google Scholar]
  3. Addison J. M., Matthews D. M., Burston D. Competition between carnosine and other peptides for transport by hamster jejunum in vitro. Clin Sci Mol Med. 1974 Jun;46(6):707–714. doi: 10.1042/cs0460707. [DOI] [PubMed] [Google Scholar]
  4. Berteloot A., Khan A. H., Ramaswamy K. Characteristics of dipeptide transport in normal and papain-treated brush border membrane vesicles from mouse intestine. II. Uptake of glycyl-L-leucine. Biochim Biophys Acta. 1982 Mar 23;686(1):47–54. doi: 10.1016/0005-2736(82)90150-x. [DOI] [PubMed] [Google Scholar]
  5. Boyd C. A., Ward M. R. A micro-electrode study of oligopeptide absorption by the small intestinal epithelium of Necturus maculosus. J Physiol. 1982 Mar;324:411–428. doi: 10.1113/jphysiol.1982.sp014121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bramhall J. Use of the fluorescent weak acid dansylglycine to measure transmembrane proton concentration gradients. Biochemistry. 1986 Jul 1;25(13):3958–3962. doi: 10.1021/bi00361a033. [DOI] [PubMed] [Google Scholar]
  7. Cheeseman C. I., Parsons D. S. The role of some small peptides in the transfer of amino nitrogen across the wall of vascularly perfused intestine. J Physiol. 1976 Nov;262(2):459–476. doi: 10.1113/jphysiol.1976.sp011605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Das M., Radhakrishnan A. N. Studies on a wide-spectrum intestinal dipeptide uptake system in the monkey and in the human. Biochem J. 1975 Jan;146(1):133–139. doi: 10.1042/bj1460133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ganapathy, Leibach F. H. Is intestinal peptide transport energized by a proton gradient? Am J Physiol. 1985 Aug;249(2 Pt 1):G153–G160. doi: 10.1152/ajpgi.1985.249.2.G153. [DOI] [PubMed] [Google Scholar]
  10. Ganapathy V., Burckhardt G., Leibach F. H. Characteristics of glycylsarcosine transport in rabbit intestinal brush-border membrane vesicles. J Biol Chem. 1984 Jul 25;259(14):8954–8959. [PubMed] [Google Scholar]
  11. Ganapathy V., Mendicino J. F., Leibach F. H. Transport of glycyl-L-proline into intestinal and renal brush border vesicles from rabbit. J Biol Chem. 1981 Jan 10;256(1):118–124. [PubMed] [Google Scholar]
  12. Ganapathy V., Mendicino J., Pashley D. H., Leibach F. H. Carrier-mediated transport of glycyl-L-proline in renal brush border vesicles. Biochem Biophys Res Commun. 1980 Dec 16;97(3):1133–1139. doi: 10.1016/0006-291x(80)91493-x. [DOI] [PubMed] [Google Scholar]
  13. Gunter-Smith P. J., Grasset E., Schultz S. G. Sodium-coupled amino acid and sugar transport by Necturus small intestine. An equivalent electrical circuit analysis of a rheogenic co-transport system. J Membr Biol. 1982;66(1):25–39. doi: 10.1007/BF01868479. [DOI] [PubMed] [Google Scholar]
  14. Hajjar J. J., Curran P. F. Characteristics of the amino acid transport system in the mucosal border of rabbit ileum. J Gen Physiol. 1970 Dec;56(6):673–691. doi: 10.1085/jgp.56.6.673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hilden S., Sacktor B. Potential-dependent D-glucose uptake by renal brush border membrane vesicles in the absence of sodium. Am J Physiol. 1982 Apr;242(4):F340–F345. doi: 10.1152/ajprenal.1982.242.4.F340. [DOI] [PubMed] [Google Scholar]
  16. Himukai M., Hoshi T. Mechanisms of glycyl-L-leucine uptake by guinea-pig small intestine: relative importance of intact-peptide transport. J Physiol. 1980 May;302:155–169. doi: 10.1113/jphysiol.1980.sp013235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Himukai M., Kameyama A., Hoshi T. Interaction of glycylglycine and Na+ at the mucosal border of guinea-pig small intestine. A non-mutual stimulation of transport. Biochim Biophys Acta. 1983 Aug 10;732(3):659–667. doi: 10.1016/0005-2736(83)90244-4. [DOI] [PubMed] [Google Scholar]
  18. Himukai M. The characteristics of carnosine transport and carnosine-induced electrical phenomena by the everted intestine of guinea pig. Jpn J Physiol. 1985;35(6):945–952. doi: 10.2170/jjphysiol.35.945. [DOI] [PubMed] [Google Scholar]
  19. Hoshi T., Komatsu Y. Sugar-evoked potential in isolated toad intestine. Jpn J Physiol. 1968 Aug 15;18(4):508–519. doi: 10.2170/jjphysiol.18.508. [DOI] [PubMed] [Google Scholar]
  20. Hoshi T. Proton-coupled transport of organic solutes in animal cell membranes and its relation to Na+ transport. Jpn J Physiol. 1985;35(2):179–191. doi: 10.2170/jjphysiol.35.179. [DOI] [PubMed] [Google Scholar]
  21. Hoshi T., Suzuki Y., Kusachi T., Igarashi Y. Interrelationship between sugar-evoked increases in transmural potential difference and sugar influxes across the mucosal border in the small intestine. Tohoku J Exp Med. 1976 Jul;119(3):201–209. doi: 10.1620/tjem.119.201. [DOI] [PubMed] [Google Scholar]
  22. Hoshi T., Takuwa N., Abe M., Tajima A. Hydrogen ion-coupled transport of D-glucose by phlorizin-sensitive sugar carrier in intestinal brush-border membranes. Biochim Biophys Acta. 1986 Oct 23;861(3):483–488. doi: 10.1016/0005-2736(86)90458-x. [DOI] [PubMed] [Google Scholar]
  23. Jentsch T. J., Janicke I., Sorgenfrei D., Keller S. K., Wiederholt M. The regulation of intracellular pH in monkey kidney epithelial cells (BSC-1). Roles of Na+/H+ antiport, Na+-HCO3(-)-(NaCO3-) symport, and Cl-/HCO3- exchange. J Biol Chem. 1986 Sep 15;261(26):12120–12127. [PubMed] [Google Scholar]
  24. Knickelbein R., Aronson P. S., Atherton W., Dobbins J. W. Sodium and chloride transport across rabbit ileal brush border. I. Evidence for Na-H exchange. Am J Physiol. 1983 Oct;245(4):G504–G510. doi: 10.1152/ajpgi.1983.245.4.G504. [DOI] [PubMed] [Google Scholar]
  25. Kohn P. G., Smyth D. H., Wright E. M. Effects of amino acids, dipeptides and disaccharides on the electric potential across rat small intestine. J Physiol. 1968 Jun;196(3):723–746. doi: 10.1113/jphysiol.1968.sp008533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lucas M. L., Schneider W., Haberich F. J., Blair J. A. Direct measurement by pH-microelectrode of the pH microclimate in rat proximal jejunum. Proc R Soc Lond B Biol Sci. 1975 Dec 31;192(1106):39–48. doi: 10.1098/rspb.1975.0150. [DOI] [PubMed] [Google Scholar]
  27. Matthews D. M., Burston D. Uptake of L-leucyl-L-leucine and glycylsarcosine by hamster jejunum in vitro. Clin Sci (Lond) 1983 Aug;65(2):177–184. doi: 10.1042/cs0650177. [DOI] [PubMed] [Google Scholar]
  28. Matthews D. M. Intestinal absorption of peptides. Physiol Rev. 1975 Oct;55(4):537–608. doi: 10.1152/physrev.1975.55.4.537. [DOI] [PubMed] [Google Scholar]
  29. Miyamoto Y., Ganapathy V., Leibach F. H. Proton gradient-coupled uphill transport of glycylsarcosine in rabbit renal brush-border membrane vesicles. Biochem Biophys Res Commun. 1985 Nov 15;132(3):946–953. doi: 10.1016/0006-291x(85)91899-6. [DOI] [PubMed] [Google Scholar]
  30. Murer H., Hopfer U., Kinne R. Sodium/proton antiport in brush-border-membrane vesicles isolated from rat small intestine and kidney. Biochem J. 1976 Mar 15;154(3):597–604. [PMC free article] [PubMed] [Google Scholar]
  31. NEWEY H., SMYTH D. H. Intracellular hydrolysis of dipeptides during intestinal absorption. J Physiol. 1960 Jul;152:367–380. doi: 10.1113/jphysiol.1960.sp006493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. NEWEY H., SMYTH D. H. The intestinal absorption of some dipeptides. J Physiol. 1959 Jan 28;145(1):48–56. doi: 10.1113/jphysiol.1959.sp006125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Preston R. L., Schaeffer J. F., Curran P. F. Structure-affinity relationships of substrates for the neutral amino acid transport system in rabbit ileum. J Gen Physiol. 1974 Oct;64(4):443–467. doi: 10.1085/jgp.64.4.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rubino A., Field M., Shwachman H. Intestinal transport of amino acid residues of dipeptides. I. Influx of the glycine residue of glycyl-L-proline across mucosal border. J Biol Chem. 1971 Jun 10;246(11):3542–3548. [PubMed] [Google Scholar]
  35. Shimada T., Hoshi T. Sodium-independent, hydrogen ion-dependent changes in membrane potential and conductance induced by dipeptides in Triturus enterocytes. Jpn J Physiol. 1986;36(3):451–465. doi: 10.2170/jjphysiol.36.451. [DOI] [PubMed] [Google Scholar]
  36. Takuwa N., Shimada T., Matsumoto H., Himukai M., Hoshi T. Effect of hydrogen ion-gradient on carrier-mediated transport of glycylglycine across brush border membrane vesicles from rabbit small intestine. Jpn J Physiol. 1985;35(4):629–642. doi: 10.2170/jjphysiol.35.629. [DOI] [PubMed] [Google Scholar]
  37. Takuwa N., Shimada T., Matsumoto H., Hoshi T. Proton-coupled transport of glycylglycine in rabbit renal brush-border membrane vesicles. Biochim Biophys Acta. 1985 Mar 28;814(1):186–190. doi: 10.1016/0005-2736(85)90435-3. [DOI] [PubMed] [Google Scholar]
  38. Taylor E., Burston D., Matthews D. M. Influx of glycylsarcosine and L-lysyl-L-lysine into hamster jejunum in vitro. Clin Sci (Lond) 1980 Mar;58(3):221–225. doi: 10.1042/cs0580221. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES